Abstract
In the present study we address the hypothesis that the basal ganglia are specifically involved in the planning of movement amplitude (or related covariates). This prediction has often been put forward based on the observation that Parkinson's disease (PD) patients exhibit hypokinesia. A close examination of the literature shows, however, that this commonly reported clinical symptom is not consistently echoed by experimental observations. When required to point to visual targets in the absence of vision of the moving limb, PD subjects exhibit various patterns of inaccuracy, including hypometria, hypermetria, systematic direction bias, or direction-dependent errors. They have even been shown to be as accurate as healthy, age-matched subjects. The main aim of the current study is to address the origin of these inconsistencies. To this end, we required nine patients presenting with advanced PD and 15 age-matched control subjects to perform planar reaching movements to visual targets. Eight targets were presented in equally spaced directions around a circle centered on the hand's starting location. Based on a previously validated parsing procedure, end-point errors were segmented into localization and planning errors. Localization errors refer to the existence of systematic biases in the estimation of the initial hand location. These biases can potentially transform a simple pattern of pure amplitude errors into a complex pattern involving both amplitude and direction errors. Results indicated that localization errors were different in the PD patients and the control subjects. This is not surprising knowing both that proprioception is altered in PD patients and that the ability to locate the hand at rest relies mainly on the proprioceptive sense, even when vision is available. Unlike normal subjects, localization errors in PD were idiosyncratic, lacking a consistent pattern across subjects. When the confounding effect of initial hand localization errors was canceled, we found that end-point errors were only due to the implementation of an underscaled movement gain (15%), without direction bias. Interestingly, the level of undershoot was found to increase with the severity of the disease (inferred from the Unified Parkinson's Disease Rating Scale, UPDRS, motor score). We also observed that movement variability was amplified (32%), but only along the main movement axis (extent variability). Direction variability was not significantly different in the patient population and the control group. When considered together, these results support the idea that the basal ganglia are specifically involved in the control of movement amplitude (or of some covariates). We propose that this structure participates in extent planning by modulating cortical activity and/or the tuning of the spinal interneuronal circuits.
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References
Adamovich SV, Berkinblit MB, Hening W, Sage J, Poizner H (2001) The interaction of visual and proprioceptive inputs in pointing to actual and remembered targets in Parkinson's disease. Neuroscience 104:1027–1041
Alexander GE, Crutcher MD (1990) Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. J Neurophysiol 64:164–178
Anderson ME, Turner RS (1991) A quantitative analysis of pallidal discharge during targeted reaching movement in the monkey. Exp Brain Res 86:623–632
Atkeson CG, Hollerbach JM (1985) Kinematic features of unrestrained vertical arm movements. J Neurosci 5:2318–2330
Bard C, Turrell Y, Fleury M, Teasdale N, Lamarre Y, Martin O (1999) Deafferentation and pointing with visual double-step perturbations. Exp Brain Res 125:410–416
Beers RJ van, Sittig AC, Denier van der Gon JJ (1996) How humans combine simultaneous proprioceptive and visual information. Exp Brain Res 111:253–261
Beers RJ van, Sittig AC, Denier van der Gon JJ (1998) The precision of proprioceptive position sense. Exp Brain Res 122:367–377
Berardelli A, Dick JP, Rothwell JC, Day BL, Marsden CD (1986) Scaling of the size of the first agonist EMG burst during rapid wrist movements in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 49:1273–1279
Berardelli A, Hallett M, Rothwell JC et al. (1996) Single-joint rapid arm movements in normal subjects and in patients with motor disorders. Brain 119:661–674
Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson's disease. Brain 124:2131–2146
Bhushan N, Shadmehr R (1999) Computational nature of human adaptive control during learning of reaching movements in force fields. Biol Cybern 81:39–60
Bock O (1992) Adaptation of aimed arm movements to sensorimotor discordance: evidence for direction-independent gain control. Behav Brain Res 51:41–50
Bock O, Arnold K (1992) Motor control prior to movement onset: Preparatory mechanisms for pointing at visual target. Exp Brain Res 90:209–216
Bock O, Arnold K (1993) Error accumulation and error correction in sequential pointing movements. Exp Brain Res 95:111–117
Bock O, Eckmiller R (1986) Goal-directed arm movements in absence of visual guidance: evidence for amplitude rather than position control. Exp Brain Res 62:451–458
Bock O, Eversheim U (2000) The mechanisms of movement preparation: a precuing study. Behav Brain Res 108:85–90
Bock O, Dose M, Ott D, Eckmiller R (1990) Control of arm movements ina two-dimensional pointing task. Exp Brain Res 40:247–250
Brotchie P, Iansek R, Horne MK (1991) Motor function of the monkey globus pallidus. 1. Neuronal discharge and parameters of movement. Brain 114:1667–1683
Carrozzo M, McIntyre J, Zago M, Lacquaniti F (1999) Viewer-centered and body-centered frames of reference in direct visuomotor transformations. Exp Brain Res 129:201–10
Crutcher MD, DeLong MR (1984) Single cell studies of the primate putamen. II. Relations to direction of movement and pattern of muscular activity. Exp Brain Res 53:244–258
Deiber MP, Ibanez V, Sadato N, Hallett M (1996) Cerebral structures participating in motor preparation in humans: a positron emission tomography study. J Neurophysiol 75:233–247
DeLong MR, Crutcher MD, Georgopoulos AP (1985) Primate globus pallidus and subthalamic nucleus: functional organization. J Neurophysiol 53:530–543
Demirci M, Grill S, McShane L, Hallett M (1997) A mismatch between kinesthetic and visual perception in Parkinson's disease. Ann Neurol 41:781–788
Denny-Brown D (1968) Clinical symptomatology of diseases of basal ganglia. In: Vinken P, Bruyn G (eds) Handbook of clinical neurology. Elsevier, New York, 6:133–171
Desmurget M, Jordan M, Prablanc C, Jeannerod M (1997) Constrained and unconstrained movements involve different control strategies. J Neurophysiol 77:1644–1650
Desmurget M, Pélisson D, Rossetti Y, Prablanc C (1998) From eye to hand: planning goal-directed movements. Neurosci Biobehav Rev 22:761–788
Desmurget M, Prablanc C, Jordan MI, Jeannerod M (1999) Are reaching movements planned to be straight and invariant in the extrinsic space: kinematic comparison between compliant and unconstrained motions. Q J Exp Psychol A 52:981–1020
Desmurget M, Vindras P, Gréa H, Viviani P, Grafton ST (2000) Proprioception does not quickly drift during visual occlusion. Exp Brain Res 134:363–377
Desmurget M, Gréa H, Grethe JS, Prablanc C, Alexander GE, Grafton ST (2001) Functional anatomy of nonvisual feedback loops during reaching: a positron emission tomography study. J Neurosci 21:2919–2928
Favilla M, Hening W, Ghez C (1989) Trajectory control in targeted force impulses. VI. Independent specification of response amplitude and direction. Exp Brain Res 75:280–294
Filion M, Tremblay L, Bedard PJ (1988) Abnormal influences of passive limb movement on the activity of globus pallidus neurons in parkinsonian monkeys. Brain Res 444:165–176
Flanders M, Helms-Tillery SI, Soechting JF (1992) Early stages in sensori-motor transformations. Behav Brain Sci 15:309–362
Flash T, Inzelberg R, Schechtman E, Korczyn AD (1992) Kinematic analysis of upper limb trajectories in Parkinson's disease. Exp Neurol 118:215–226
Flowers KA (1976) Visual "closed-loop" and "open-loop" characteristics of voluntary movement in patients with parkinsonism and intention tremor. Brain 99:269–310
Georgopoulos AP (1995) Current issues in directional motor control. Trends Neurosci 18:506–510
Georgopoulos AP, Delong MR, Crutcher MD (1983) Relations between parameters of step-tracking movements and single cells discharge in the globus pallidus and subthalamic nucleus of the behaving monkey. J Neurosci 3:1586–1598
Ghez C, Favilla M, Ghilardi MF, Gordon J, Bermejo R, Pullman S (1997) Discrete and continuous planning of hand movements and isometric force trajectories. Exp Brain Res 115:217–233
Ghilardi MF, Alberoni M, Rossi M, Franceschi M, Mariani C, Fazio F (2000) Visual feedback has differential effects on reaching movements in Parkinson's and Alzheimer's disease. Brain Res 876:112–123
Godaux E, Koulischer D, Jacquy J (1992) Parkinsonian bradykinesia is due to depression in the rate of rise of muscle activity. Ann Neurol 31:93–100
Goodale MA, Pélisson D, Prablanc C (1986) Large adjustments in visually guided reaching do not depend on vision of the hand and perception of target displacement. Nature 320:748–750
Gordon J, Ghilardi MF, Ghez C (1994) Accuracy of planar reaching movements. 1. Independence of direction and extent variability. Exp Brain Res 99:97–111
Hallett M, Khoshbin S (1980) A physiological mechanism of bradykinesia. Brain 103:301–314
Hamada I, DeLong MR, Mano N (1990) Activity of identified wrist-related pallidal neurons during step and ramp wrist movements in the monkey. J Neurophysiol 64:1892–1906
Hays WL (1988) Statistics, 4th edn. Holt, Rinehart and Winton, Fort Worth
Higgins JR, Angel RW (1970) Correction of tracking errors without sensory feedback. J Exp Psychol 84:412–416
Jaeger RJ, Agarwal GC, Gottlieb GL (1979) Directional errors of movement and their correction in a discrete tracking task. J Mot Behav 11:123–133
Jaric S, Corcos DM, Latash M (1992) Effects of practice on final position reproduction. Exp Brain Res 91:129–134
Jeannerod M (1988) The neural and behavioral organization of goal-directed movements. Clarendon, Oxford
Jobst EE, Melnick ME, Byl NN, Dowling GA, Aminoff MJ (1997) Sensory perception in Parkinson disease. Arch Neurol 54:450–454
Johnson MT, Kipnis AN, Lee MC, Loewenson RB, Ebner TJ (1991) Modulation of the stretch reflex during volitional sinusoidal tracking in Parkinson's disease. Brain 114:443–460
Johnson RA, Wichern DW (1982) Applied multivariate statistical analysis. Prentice Hall, Englewood Cliffs, NJ
Kalaska JF, Crammond DJ (1992) Cerebral cortical mechanisms of reaching movements. Science 255:1517–1523
Klockgether T, Dichgans J (1994) Visual control of arm movement in Parkinson's disease. Mov Disord 9:48–56
Klockgether T, Borutta M, Rapp H, Spieker S, Dichgans J (1995) A defect of kinesthesia in Parkinson's disease. Mov Disord 10:460–465
Krakauer JW, Pine ZM, Ghilardi MF, Ghez C (2000) Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci 20:8916–8924
Lawrence AD (2000) Error correction and the basal ganglia: similar computations for action, cognition and emotion? Trends Cogn Sci 4:365–367
McIntyre J, Stratta F, Droulez J, Lacquaniti F (2000) Analysis of pointing errors reveals properties of data representations and coordinate transformations within the central nervous system. Neural Comput 12:2823–2855
Messier J, Kalaska JF (1997) Differential effect of task conditions on errors of direction and extent of reaching movements. Exp Brain Res 115:469–478
Meunier S, Pol S, Houeto JL, Vidailhet M (2000) Abnormal reciprocal inhibition between antagonist muscles in Parkinson's disease. Brain 123:1017–1026
Mink JW, Thach WT (1991) Basal ganglia motor control. II. Late pallidal timing relative to movement onset and inconsistent pallidal coding of movement parameters. J Neurophysiol 65:301–329
Moore A (1987) Impaired sensorimotor integration in Parkinsonism and dyskinesia: a role for corollary discharges? J Neurol Neurosurg Psychiatry 50:544–552
Morasso P (1981) Spatial control of arm movements. Exp Brain Res 42:223–227
Morita H, Shindo M, Ikeda S, Yanagisawa N (2000) Decrease in presynaptic inhibition on heteronymous monosynaptic Ia terminals in patients with Parkinson's disease. Mov Disord 15:830–834
Nambu A, Yoshida S, Jinnai K (1990) Discharge patterns of pallidal neurons with input from various cortical areas during movement in the monkey. Brain Res 519:183–191
Pélisson D, Prablanc C, Goodale MA, Jeannerod M (1986) Visual control of reaching movements without vision of the limb. II. Evidence of fast unconscious processes correcting the trajectory of the hand to the final position of a double step stimulus. Exp Brain Res 62:303–311
Petit H, Allain H, Vermersch P (1995) La maladie de Parkinson. Masson, Paris
Pfann KD, Buchman AS, Comella CL, Corcos DM (2001) Control of movement distance in Parkinson's disease. Mov Disord 16:1048–1065
Phillips JG, Martin KE, Bradshaw JL, Iansek R (1994) Could bradykinesia in Parkinson's disease simply be compensation? J Neurol 241:439–447
Pine ZM, Krakauer JW, Gordon J, Ghez C (1996) Learning of scaling factors and reference axes for reaching movements. Neuroreport 7:2357–2361
Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67:455–69
Redon C, Hay L, Velay JL (1991) Proprioceptive control of goal directed movements in man studied by means of vibratory muscle tendon stimulation. J Mot Behav 23:101–108
Rosenbaum DA (1980) Human movement initiation: specification of arm direction and extent. J Exp Psychol Gen 109:444–474
Rossetti Y, Desmurget M, Prablanc C (1995) Vectorial coding of movement: Vision proprioception or both? J Neurophysiol 74:457–463
Sainburg RL, Lateiner JE, Latash ML, Bagesteiro LB (2003) Effects of altering initial position on movement direction and extent. J Neurophysiol 89:401–415
Sanes JN (1985) Information processing deficits in Parkinson's disease during movement. Neuropsychologia 23:381–392
Schneider JS, Diamond SG, Markham CH (1987) Parkinson's disease: sensory and motor problems in arms and hands. Neurology 37:951–956
Sheridan MR, Flowers KA (1990) Movement variability and bradykinesia in Parkinson's disease. Brain 113:1149–1161
Siebner HR, Limmer C, Peinemann A, Bartenstein P, Drzezga A, Conrad B (2001) Brain correlates of fast and slow handwriting in humans: a PET-performance correlation analysis. Eur J Neurosci 14:726–736
Smith MA, Brandt J, Shadmehr R (2000) Motor disorder in Huntington's disease begins as a dysfunction in error feedback control. Nature 403:544–549
Teasdale N, Phillips J, Stelmach GE (1990) Temporal movement control in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 53:862–868
Turner RS, Anderson ME (1997) Pallidal discharge related to the kinematics of reaching movements in two dimensions. J Neurophysiol 77:1051–1074
Turner RS, Grafton ST, Votaw JR, DeLong MR, Hoffman JM (1998) Motor subcircuits mediating the control of movement velocity: a PET study. J Neurophysiol 80:2162–2176
Vindras P, Viviani P (1998) Frames of reference and control parameters in visuomanual pointing. J Exp Psychol Hum Percept Perform 24:569–591
Vindras P, Viviani P (2002) Altering the visuo-motor gain: evidence that motor plans deal with vector quantities. Exp Brain Res 147:280–295
Vindras P, Desmurget M, Prablanc C, Viviani P (1998) Pointing errors reflect biases in the perception of the initial hand position. J Neurophysiol 79:3290–3294
Wann JP, Ibrahim SF (1992) Does limb proprioception drift? Exp Brain Res 91:162–166
Wichmann T, DeLong MR (1996) Functional and pathophysiological models of the basal ganglia. Curr Opin Neurobiol 6:751–758
Won J, Hogan N (1995) Stability properties of human reaching movements. Exp Brain Res 107:125–136
Zia S, Cody F, O'Boyle D (2000) Joint position sense is impaired by Parkinson's disease. Ann Neurol 47:218–228
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Supported by NIH grants NS33704 and NS37470.
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Desmurget, M., Grafton, S.T., Vindras, P. et al. Basal ganglia network mediates the control of movement amplitude. Exp Brain Res 153, 197–209 (2003). https://doi.org/10.1007/s00221-003-1593-3
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DOI: https://doi.org/10.1007/s00221-003-1593-3